Hardening of bio-silica in sponge spicules involves an aging process after its enzymatic polycondensation: Evidence for an aquaporin-mediated water absorption

Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid an...

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Published inBiochimica et biophysica acta Vol. 1810; no. 7; pp. 713 - 726
Main Authors Müller, Werner E.G., Wang, Xiaohong, Wiens, Matthias, Schloßmacher, Ute, Jochum, Klaus Peter, Schröder, Heinz C.
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.07.2011
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Abstract Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial. Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies. Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited. This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material. ► Sponges as a model system for evolution of metazoan body plans. ► Sponges as a model system for basic studies of skeleton formation in animals. ► Enzymatic polycondensation reaction for the formation of bio-silica. ► Expression of aquaporin gene for the first time shown during bio-silica formation. ► First description that bio-silica formation in animals requires a de-hydration step.
AbstractList Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial.BACKGROUNDSpicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial.Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies.METHODSCell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies.Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited.RESULTSCell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited.This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material.GENERAL SIGNIFICANCEThis study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material.
Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial. Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies. Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited. This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material.
BACKGROUND: Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial. METHODS: Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies. RESULTS: Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited. GENERAL SIGNIFICANCE: This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material.
Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes their inorganic matrix. It remained unexplored which reactions are involved in molding of the amorphous bio-silica and formation of a solid and rigid biomaterial. Cell and molecular biological techniques have been applied to analyze processes resulting in the hardening of the enzymatically synthesized bio-silica. The demosponge Suberites domuncula has been used for the studies. Cell aggregates (primmorphs) from the sponge S. domuncula, grown in the presence of Mn-sulfate, form spicules that comprise, instead of a smooth, a rough and porous surface which is decorated with irregular bio-silica deposits. During this process, the expression of the aquaporin-8 gene becomes down-regulated. Further in vitro studies showed that aquaporin is required for dehydration, and hardening of bio-silica following its enzymatic formation. The data show that in cell aggregates grown in the presence of Mn-sulfate, aquaporin-8 is down-regulated. We conclude that in cell aggregates grown in the presence of Mn-sulfate, the removal of reaction water, produced during the bio-silica polycondensation reaction, is inhibited. This study highlights that besides the silicatein-driven polycondensation reaction, the spicule formation also requires a phase of syneresis that results in a hardening of the material. ► Sponges as a model system for evolution of metazoan body plans. ► Sponges as a model system for basic studies of skeleton formation in animals. ► Enzymatic polycondensation reaction for the formation of bio-silica. ► Expression of aquaporin gene for the first time shown during bio-silica formation. ► First description that bio-silica formation in animals requires a de-hydration step.
Author Müller, Werner E.G.
Wang, Xiaohong
Jochum, Klaus Peter
Schloßmacher, Ute
Wiens, Matthias
Schröder, Heinz C.
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  givenname: Ute
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  givenname: Heinz C.
  surname: Schröder
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  organization: ERC Advanced Grant Research Group at the Institute for Physiological Chemistry, University Medical Center of the Johannes Gutenberg University, Duesbergweg 6, D-55128 Mainz, Germany
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Keywords AQP
Mn
Bio-silica
qRT-PCR
DAPI
Sponges
IEF
Spicules
Primmorphs
Hardening
Cu
TEOS
PEG
Zn
EDX
SEM
Suberites domuncula
HF
PCR
Fe
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Snippet Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica, constitutes...
BACKGROUND: Spicules, the siliceous skeletal elements of the siliceous sponges, are synthesized enzymatically via silicatein. The product formed, bio-silica,...
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SubjectTerms absorption
Absorption - drug effects
Amino Acid Sequence
Animals
aquaporins
Aquaporins - classification
Aquaporins - genetics
Aquaporins - metabolism
Bio-silica
Cathepsins - genetics
Cathepsins - metabolism
cell aggregates
Fluorescent Antibody Technique
Gene Expression - drug effects
gene expression regulation
genes
Hardening
in vitro studies
Magnesium Sulfate - pharmacology
Microscopy, Electron, Scanning
Molecular Sequence Data
Phase Transition - drug effects
Phylogeny
Primmorphs
Reverse Transcriptase Polymerase Chain Reaction
Sequence Homology, Amino Acid
Silicon Dioxide - chemistry
Silicon Dioxide - metabolism
Spectrometry, X-Ray Emission
Spicules
Sponges
Suberites - genetics
Suberites - metabolism
Suberites - ultrastructure
Suberites domuncula
Time Factors
Water - metabolism
Title Hardening of bio-silica in sponge spicules involves an aging process after its enzymatic polycondensation: Evidence for an aquaporin-mediated water absorption
URI https://dx.doi.org/10.1016/j.bbagen.2011.04.009
https://www.ncbi.nlm.nih.gov/pubmed/21565255
https://www.proquest.com/docview/2000019670
https://www.proquest.com/docview/878593432
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